Sulfidogenic activity of sulfate and sulfur reducing bacteria under the influence of metal compounds

O. M. Moroz; S. O. Hnatush; O. V. Tarabas; C. I. Bohoslavets; G. V. Yavorska; B. M. Borsukevych

doi:10.15421/011801

O. M. Moroz Ivan Franko National University of Lviv http://orcid.org/0000-0002-6494-8648
S. O. Hnatush Ivan Franko National University of Lviv http://orcid.org/0000-0002-5353-102X
O. V. Tarabas Ivan Franko National University of Lviv http://orcid.org/0000-0003-4289-0171
C. I. Bohoslavets Ivan Franko National University of Lviv
G. V. Yavorska Ivan Franko National University of Lviv http://orcid.org/0000-0002-0641-0794
B. M. Borsukevych Ivan Franko National University of Lviv http://orcid.org/0000-0002-8912-8064

Keywords: Desulfovibrio; Desulfuromonas; heavy metals; hydrogen sulfide

Abstract

Due to their high content in natural environments, heavy metals exhibit toxic effects on living organisms, which leads to a decrease in the biological diversity and productivity of ecosystems. In niches with low oxidation reducing potential, sulfate and sulfur reducing bacteria carry out the reducing transformation of oxidized sulfur compounds with the formation of significant amounts of hydrogen sulfide. H2S produced by bacteria interacts with metal ions, precipitating them in the form of sulfides. The aim of this work was to investigate the influence of lead, cuprum (II), iron (II) and manganese (II) salts on the production of hydrogen sulfide by bacteria of the Desulfovibrio and Desulfuromonas genera, isolated from Yavorivske Lake, and to evaluate the efficiency of their use for purifying media, enriched with organic compounds, from hydrogen sulfide and heavy metals. The content of heavy metal ions in the water of Yavorivske Lake was determined by the spectrophotometric method. The bacteria were grown for 10 days at 30 °C in the Kravtsov-Sorokin medium under anaerobic conditions. To study the influence of metal ions on bacteria growth and their H2S production, cells were incubated with metal salts (0.5–4.0 mM), washed and grown in media with SO42– or S0. To determine the level of metal ions binding by H2S, produced by bacteria, cells were grown in media with metal compounds (0.5–4.0 mM), SO42– or S0. Biomass was determined by turbidimetric method. In the cultural liquid the content of H2S was determined quantitatively by spectrophotometric method, and qualitatively by the presence of metal cations. The content of metal sulfides in the growth medium was determined by weight method. Sulfate and sulfur-reducing bacteria were resistant to 2.0 mM Pb(NO3)2, 2.5 mM CuCl2, 2.5 mM FeCl2 × 4H2O and 2.0 mM MnCl2 × 4H2O, therefore they are promising for the development of biotechnologies for the purification of water resources contaminated by sulfur and metal compounds. When present in a medium with sulfates or sulfur of 1.0–1.5 mM lead, cuprum (II), iron (II) or manganese (II) ions, they almost completely bind with the H2S produced by bacteria in the form of insoluble sulfides, which confirms the negative results of qualitative reactions to their presence in the cultural liquid.

References

Baran, I. M., Podopryhora, O. I., Gryshchuk, G. V., Bondar, L. S., Kit, L. Y., Klym, I. R., Нnatush, S. O., & Gudz, S. P. (2003). Ekolohichnyy monitorynh vodoym Yavorivs'koho sirkovoho rodovyshcha; mikrobiolohichnyy kontrol' [The ecological monitoring of Yavoriv sulfur deposit reservoirs; microbiological control]. Environment and Health, 27(4), 56–62 (in Ukrainian).

Bilyy, O. I. Vasyliv, O. M., & Hnatush, S. O. (2014). The anode biocatalyst with simultaneous transition metals pollution control. Technology and Application of Microbial Fuel Cells. InTech, Rijeka, Croatia.

Cologgi, D. L., Lampa-Pastirk, S., Speers, A. M., Kelly, S. D., & Reguera, G. (2011). Extracellular reduction of uranium via Geobacter conductive pili as a protective cellular mechanism. Proceedings of the National Academy of Sciences of the United States of America, 108, 15248–15252.

Dey, U., Chatterjee, S., & Mondal, N. K. (2016). Isolation and characterization of arsenic-resistant bacteria and possible application in bioremediation. Biotechnology Reports, 10, 1–7.

Eger, P. (1994). Wetland treatment for trace metal removal from mine drainage: The importance of aerobic and anaerobic processes. Water Science and Technology, 29(1), 249−256.

Fitzgeralda, L. A., Petersenb, E. R., Learyc, D. H., Nadeaud, L. J., Sotoe, C. M., Rayf, R. I., Littlef, B. J., Ringeisena, B. R., Johnsond, G. R., Vorae, G. J., & Biffingera, J. C. (2013). Shewanella frigidimarina microbial fuel cells and the influence of divalent cations on current output. Biosensors and Bioelectronics, 40(1), 102–109.

Frank, Y. A., & Lushnikov, S. V. (2006). Biotekhnologicheskij potencial sul'fatreduciruyushchih bakterіj [Biotechnological potential of sulfate reducing bacteria]. Ehkologiya i Promyshlennost', 1, 10–13 (in Russian).

Gaidin, A. M., & Zozulia, I. I. (2009). Novi ozera L'vivshchyny [New lakes of Lviv region]. Afisha, L'viv (in Ukrainian).

Grushko, Y. M. (1979). Vrednye neorganicheskie soedineniya v promyshlennyh stochnyh vodah [Harmful inorganic compounds in industrial wastewater]. Himiya, Leningrad (in Russian).

Gudz, S. P., Нnatush, S. O., Moroz, O. M., Peretiatko, T. B., & Vasyliv, O. M. (2013). Svidotstvo pro deponuvannya shtamu bakteriy Desulfuromonas acetoxidans Ya-2006 u Depozytariyi Instytutu mikrobiolohiyi i virusolohiyi im. D. K. Zabolotnoho NAN Ukrayiny z nadannyam reyestratsiynoho nomeru IMV V-7384 [Certificate of deposition of bacteria Desulfuromonas acetoxidans Ya-2006 strain in the Depository of D. K. Zabolotny Institute of Microbiology and Virology of the NAS of Ukraine with appropriation of registration number IMV V-7384] (in Ukrainian).

Gudz, S., Нnatush, S., Peretiatko, T., Palianytsia, B., Kostruba, M., Podopryhora, O., & Klym, I. (2004). Dynamika zmin tytru sulʹfatvidnovlyuvalʹnykh bakteriy ta vmistu sulʹfativ i sirkovodnyu u vodakh kar’yeru Yavorivsʹkoho sirkovoho rodovyshcha v protsesi yoho zatoplennya [Dynamics of changes in the titres of sulfate reducing bacteria and the content of sulfates and hydrogen sulfide in the waters of the Yavoriv sulfur deposit in the course of its flooding]. Visnyk of L’viv University. Biological Series, 37, 185−189 (in Ukrainian).

Gudz, S. P., Нnatush, S. O., Yavorska, G. V., Bilinska, I. S., & Borsukevych, B. M. (2014). Praktykum z mikrobiologii' [Workshop on microbiology]. Ivan Franko National University of L’viv, Lviv (in Ukrainian).

Gudz, S. P., Peretiatko, T. B., Moroz, O. M., Hnatush, S. O., & Klym, I. R. (2011). Rehulyuvannya rivnya sul'fativ, sirkovodnyu ta vazhkykh metaliv u tekhnohennykh vodoymakh sulfatvidnovljuval'nymy bakterijamy [Regulation of sulfates, hydrogen sulfide and hard metals level in technogenic reservoirs by sulfate reducing bacteria]. Mikrobiologichny Zhurnal, 73(2), 33–38 (in Ukrainian).

Hao, O. J. (2000). Metal effects on sulfur cycle bacteria and metal removal by sulfate-reducing bacteria. Environmental technologies to treat sulfur pollution. Principles and engineering. IWA Publishing, London.

Harris, D. S. (2003). Quantitative chemical analysis. Amazon, New York.

Hedderich, R., Klimmek, O., Kroger, A., Dirmeier, R., Keller, M., & Stetter, K. O. (1999). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiology Reviews, 22(5), 353–381.

Iwahori, K., Watanabe, J., Tani, Y., Seyama, H., & Miyata, N. (2014). Removal of heavy metal cations by biogenic magnetite nanoparticles produced in Fe(III)-reducing microbial enrichment cultures. Journal of Bioscience and Bioengineering, 117(3), 333–335.

Kiran, M. G., Pakshirajan, K., & Das, G. (2017). Heavy metal removal from multicomponent system by sulfate reducing bacteria: Mechanism and cell surface characterization. Journal of Hazardous Materials, 324(PtA), 62−70.

Kozlova, I. P., Radchenko, O. S., Stepura, L. H., Kondratyuk, T. O., & Pilyashenko-Novokhatnyy, A. I. (2008). Heokhimichna diyalʹnistʹ mikroorhanizmiv ta yiyi prykladni aspekty [Geochemical activity of microorganisms and its applied aspects]. Naukova Dumka, Kyiv (in Ukrainian).

Kushkevych, I., Нnatush, S., & Gudz, S. (2007). Vplyv vazhkykh metaliv na klityny mikroorhanizmiv [The influence of heavy metals on microorganism cells]. Visnyk of L’viv University. Biological Series, 45, 3–28 (in Ukrainian).

Kuzmishyna-Diakiv, S., & Hnatush, S. (2015). Microbiota of the coal pits waste heaps. OmniScriptum GmbH & Co. KG, Lambert Academic Publishing, Saarbrücken, Germany.

Kuzmishyna, S. V., Нnatush, S. O., & Halushka, A. A. (2015). Mikrobiota porodnykh vidvaliv vuhilʹnykh shakht Chervonohradsʹkoho hirnychopromyslovoho rayonu za vnesennya zoly [Microbiota of the coal pit waste heaps of Chervonograd mining region after coal ash applying]. Visnyk of Dnipropetrovsk University. Biology, Ecology, 23(1), 33−38 (in Ukrainian).

Kuznetsov, A., Gradova, N., Lushnikov, S., Éngelkhart, M., Vaysser, T., & Chebotareva, M. (2015). Prikladnaya ehkobiotekhnologiya [Applied Ecobiotechnology]. Binom Laboratoriya Znanij, Moscow (in Russian).

Lengeler, J., Drevs, G., & Shlegel, G. (Eds.). (2005). Sovremennaya mikrobiologiya. Prokarioty [Contemporary Microbiology. Prokaryotes]. Mir, Moscow (in Russian).

Limcharoensuk, T., Sooksawat, N., Sumarnrote, A., Awutpet, T., Kruatrachue, M., Pokethitiyook, P., & Auesukaree, C. (2015). Bioaccumulation and biosorption of Cd²⁺ and Zn²⁺ by bacteria isolated from a zinc mine in Thailand. Ecotoxicology and Environmental Safety, 122, 322–330.

Lovley, D. (2006). Dissimilatory Fe(III)- and Mn(IV)-reducing prokaryotes. The Procaryotes. Springer-Verlag, LLC, New York.

Maslovska, O., & Hnatush, S. (2015). Oxidative modification of proteins and specific superoxide dismuase activity of Desulfuromonas acetoxidans ІМV В-7384 bacteria under the influence of ferric citrate. Microbiology and Biotechnology, 30, 34−40.

McEldowney, S. (1990). Microbial biosorbtion of radionuclides in liquid effluent treatment. Applied Biochemistry and Biotechnology, 5, 159–179.

Moroz, O. M. (2010). Zakonomirnosti utvorennya sirkovodnyu sulfatvidnovlyuvalnymy bakteriyamy vodoymy karyeru Yavorivskoho sirkovoho rodovyshcha [Regularities of hydrogen sulfide production by sulfate reducing bacteria from water of Yavoriv sulfur deposit open pit]. Scientific Bulletin of the Uzhgorod University. Series Biology, 27, 56–63 (in Ukrainian).

Moroz, O. M., Kolisnyk, Y. I., Podopryhora, O. I., Klym, I. R., Gudz, S. P., Borsukevych, B. M., & Hnatush, S. O. (2008). Mikroflora vody ozera “Yavorivske” [Microflora of lake “Javorivske” water]. Scientific Bulletin of the Uzhgorod University. Series Biology, 24, 131–138 (in Ukrainian).

Moroz, O. M., Peretiatko, T. B., Klym, I. R., Borsukevych, B. M., Yavorska, G. V., Kulachkovsky, O. R. (2013). Sirkovidnovlyuvalni bakteriyi ozera Yavorivske: Deyaki morfolohichni, kulturalni i fiziolohichni osoblyvosti [Sulfur reducing bacteria from Yavorivske lake: Some morphological, cultural and physiological peculiarities]. Scientific Bulletin of the Uzhgorod University. Series Biology, 35, 34–41 (in Ukrainian).

Moroz, O. M. (2013). Utvorennya hidrohen sulfidu sirkovidnovlyuvalnymy bakteriyamy za vplyvu soley vazhkykh metaliv [Formation of hydrogen sulfide by sulfur reducing bacteria under the influence of heavy metal salts]. Visnyk of L’viv University. Biological Series, 61, 154–165 (in Ukrainian).

Moroz, O. M., Hnatush, S. O., Bohoslavets, C. I., Yavorska, G. V., & Truchym, N. V. (2016). Vykorystannya bakteriyamy Desulfuromonas sp. yoniv ferumu (III) i manhanu (IV) yak aktseptoriv elektroniv [Usage of ferrum (ІІІ) and manganese (IV) ions as electron acceptors by bacteria of Desulfuromonas sp.]. Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(1), 87−95 (in Ukrainian).

Moroz, O. M., Hnatush, S. O., Bohoslavets, C. I., Hrytsun’, T. M., & Borsukevych, B. M. (2017). Vplyv kaliy bikhromatu na dysymilyatsiyne vidnovlennya yoniv sulfatu i nitratu bakteriyamy Desulfovibrio sp. [The influence of potassium dichromate on dissimilatory reduction of sulfate and nitrate ions by bacteria Desulfovibrio sp.]. Ecology and Noospherology, 28(1−2), 84−95 (in Ukrainian).

Mustapha, M. U., & Halimoon, N. (2015). Screening and isolation of heavy metal tolerant bacteria in industrial effluent. Procedia Environmental Sciences, 30, 33–37.

Peretiatko, T., Gudz, S., & Halushka, A. (2009a). Vykorystannya metaliv yak kintsevykh aktseptoriv elektroniv sulfatvidnovlyuvalnymy bakteriyamy [The use of metals as final electron acceptors by sulfate reducing bacteria]. Biolohichni Studiyi, 3(3), 141–158 (in Ukrainian).

Peretiatko, T. B., Halushka, A. A., Gudz, S. P., & Нnatush, S. O. (2009b). Svidotstvo pro deponuvannya asociatsii sulfatvidnovliuvalnych bakteriy Ya-11 (Desulfovibrio desulfuricans Ya-11 i Pseudomonas sp.) u Depozytariyi Instytutu Mikrobiolohiyi i Virusolohiyi im. D. K. Zabolotnoho NAN Ukrayiny z nadannyam reyestratsiynoho nomeru IMV K-6 [Certificate of deposition of bacteria Ya-11 (Desulfovibrio desulfuricans Ya-11 and Pseudomonas sp.) association in the Depository of D. K. Zabolotny Institute of Microbiology and Virology of the NAS of Ukraine with appropriation of registration number IMV K-6] (in Ukrainian).

Rabus, R., Venceslau, S. S., Wöhlbrand, L., Voordouw, G., Wall, J. D., & Pereira, I. A. C. (2015). A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes. Chapter Two. Advances in Microbial Physiology, 66, 55–321.

Richter, K., Schicklberger, M. & Gescher, J. (2012). Dissimilatory reduction of extracellular electron acceptors in anaerobic respiration. Applied Environmental Microbiology, 78(4), 913–921.

Roane, T. M. (1999). Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microbial Ecology, 37, 218−224.

Saffarini, D. (2015). Metabolism of metals and metalloids by the sulfate-reducing bacteria. Bacteria-metal interactions. Springer International Publishing, Switzerland.

Segin, T., Hnatush, S., & Gorishniy, M. (2016). Protsesy lipoperoksydatsiyi u klitynakh Chlorobium limicola IMV K-8 za vplyvu Cu (II) sulfatu [Lipoperoxidation processes in Chlorobium limicola IMV K-8 cells under the influence of Cu (II) sulfate]. Visnyk of Dnipropetrovsk University. Biology, Ecology, 24(1), 72−78 (in Ukrainian).

Si, Y., Zou, Y., Liu, X., Si, X., & Mao, J. (2015). Mercury methylation coupled to iron reduction by dissimilatory iron-reducing bacteria. Chemosphere, 122, 206–212.

Silver, S., & Walderhaug, M. (1995). Bacterial plasmid-mediated resistances to mercury, cadmium and copper. Toxicology of Metals. Biochemical Aspects. Springer, Berlin.

Smirnova, G. F., & Podgorsky, V. S. (2013). Vosstanovlenie hromatov Pseudomonas sp. sht. 10 v prisutstvii nekotoryh tjazhjolyh metallov i al'ternativnyh akceptorov jelektronov [Chromates reducing by Pseudomonas sp. str. 10 in presence of some heavy metals and alternative electron acceptors]. Mikrobiologichny Zhurnal, 75(4), 8–12 (in Russian).

Solioz, M., & Stoyanov, J. (2003). Copper homeostasis in Enterococcus hirae. FEMS Microbiology Reviews, 27(2−3), 183−195.

Tarabas, O., Moroz, O., Hnatush, S., Yavorska, G., Zvir, G., & Kovalchuk, M. (2017). Ekoloho-trofichni hrupy mikroorhanizmiv vody ozera Yavorivske [Ecological trophic groups of microorganisms of Yavorivske lake water]. Visnyk of L’viv University. Biological Series, 76, 166−178 (in Ukrainian).

Vasyliv, O., Bilyy, O., Hnatush, S., Kushkevych, I., & Getman, V. (2011). The changes of spectroscopic characteristics of sulfur reducing bacteria Desulfuromonas acetoxidans under the influence of different metal ions. Proceedings of SPIE, 8152, 81520B–1–7.

Vasyliv, O., & Hnatush, S. (2013). Vplyv spoluk perekhidnykh metaliv na aktyvnist superoksyddysmutazy sirkovidnovlyuvalnykh bakteriy Desulfuromonas acetoxidans [Influence of transition metal compounds on the activity of superoxide dismutase of sulfur reducing bacteria Desulfuromonas acetoxidans]. Mikrobiologichny Zhurnal, 75(2), 37–44 (in Ukrainian).

Viti, C., Marchi, E., Decorosi, F., & Giovannetti, L. (2014). Molecular mechanisms of Cr (VI) resistance in bacteria and fungi. FEMS Microbiology Reviews, 38(4), 633–659.

Wang, Q., Ding, D., Hu, E., Yu, R., & Qiu, G. (2008). Removal of SO₄²⁻, uranium and other heavy metal ions from simulated solution by sulfate reducing bacteria. Transactions of Nonferrous Metals Society of China, 18(6), 1529–1532.

Wang, W., Feng, Y., Tang, X., Li, H., Du, Z., Yi, A., & Zhang, X. (2015). Enhanced U(VI) bioreduction by alginate-immobilized uranium-reducing bacteria in the presence of carbon nanotubes and anthraquinone-2,6-disulfonate. Journal of Environmental Sciences, 31, 68–73.

White, C., Sayer, J. A., & Gadd, G. M. (2000). Microbial solubilization and immobilization of toxic metals: Key biogeochemical processes for treatment of contamination. FEMS Microbiology Ecology, 33, 197–208.

Wilkins, M. J., Callister, S. J., Miletto, M., Williams, K. H., Nicora, C. D., Lovley, D. R., Long, P. E., & Lipton, M. S. (2011). Development of a biomarker for Geobacter activity and strain composition; proteogenomic analysis of the citrate synthase protein during bioremediation of U (VI). Microbial Biotechnology, 4(1), 55−63.

Winkelmann, G. (Ed). (2002). Microbial transport systems. Wiley-Vch, New York.

Yavorska, G. V., Gudz, S. P., & Нnatush, S. O. (2008). Promyslova mikrobiolohiya [Industrial microbiology]. Publishing Center of Ivan Franko National University of Lviv, Lviv (in Ukrainian).

Zhuang, K., Ma, E., Lovley, D. R., & Mahadevan, R. (2012). The design of long-term effective uranium bioremediation strategy using a community metabolic model. Biotechnology and Bioengineering, 109(10), 2475−2483.

Sulfidogenic activity of sulfate and sulfur reducing bacteria under the influence of metal compounds

Abstract

References

Most read articles by the same author(s)